Influence of shift work on periodontitis according to the occupation group

This study aimed to investigate the effects of shift work on periodontal disease in blue-and white-collar workers and to examine the interaction effects between occupation and work patterns. Data were collected from the Korea National Health and Nutrition Examination Survey conducted by the Korean Ministry of Health and Welfare for a total of nine years from 2007 to 2015. Participants with missing outcome variables were excluded from the analysis and a total of 32,336 participants were included in the final analysis. Univariable odds ratios (OR) were calculated using a logistic regression model with 95% confidence interval (CI). A multivariable logistic regression analysis was performed using the backward elimination method. The CONTRAST statement was used to analyze the interaction effect between occupation and work patterns. Multivariable logistic regression analysis revealed that interaction effects are present between the terms, occupational type and work pattern. Crude OR of shift work for periodontitis was 1.269 [CI 1.213–1.327, P < 0.05]. However, following adjustment for multiple confounding factors and the interaction effect term considered, this OR (1.269) increased to 1.381 [CI 1.253–1.523] in white-collar group while it decreased to 1.198 [1.119–1.283] in blue-collar. Crude OR of blue-collar (OR = 3.123, CI 2.972–3.281, P < 0.05) decreased to 1.151 [CI 1.049–1.262] when interaction effect to the shift work was considered. Shift work pattern increases the risk for periodontitis and this adverse effect is greater when white-collar workers are engaged comparing to blue-collar. The result of this study suggests that 24/7 lifestyle of the modern society poses health risks to the relevant people and the potential harm can be greater to white-collar workers.


Shift work and related sleep disorder
Shift work refers to a type of work being performed during outside of regular daytime hours, i.e., 09:00-18:00.Occupations engaging in 24-h restaurants, convenience stores, hospitals, and delivery work are the fields that are closely related to shift work.Shift workers may need alterations in their original sleep pattern in order to comply with shift work schedules and this leads to various systemic illnesses that are developed among shift workers 2 .
This biological harm can be primarily explained by circadian rhythmicity inherent in every organ and system of our body.When circadian disruption is occurred by atypical sleep pattern, metabolism and/or immunologic

Aim of the study
Therefore, our next question was which specific type of the occupation is mostly affected by shift work in terms of periodontal health.So called, white-collar and blue-collar jobs differ significantly in terms of the amount of physical demand, daily smoking, or dietary habits of the workers, and therefore, risk for various systemic diseases [11][12][13] .Blue-collar workers are more vulnerable to cancer, cardiovascular disease, and depressive disorders compared to other industries and job types 13 .On the other hand, white-collar workers are more prone to be exposed to psychosocial stresses at work showing higher prevalence for uncontrolled hypertension 11 .In term of periodontal health, blue-collar workers are found to have higher odds ratio for complete tooth loss in Japanese population 14 .Another population study in South Korea also revealed that blue-collar workers are more prone to have periodontal disease 15 .Since white-collar workers generally deal with psychologically-demanding tasks and large part of their work is done in front of the computer screen where blue-light is engaged, it was our hypothesis that SWSD may affect white-collar workers more strongly.The null hypothesis of this study was that shift work and the related sleep disorders does not affect periodontitis depending on the occupational type.

Survey participants
The data used in this study were derived from the Korea National Health and Nutrition Examination Survey, a nationwide cross-sectional survey conducted by the Korean Ministry of Health and Welfare between 2007 and 2015.The inclusion criteria were participants aged ≥ 19 years and those who answered the questionnaire regarding the longest occupation they had during their lifetime.Participants without records of work patterns or periodontal status were excluded from the study.
Of the 73,353 study participants, 56,039 were aged 19 years or older and 47,942 responded to the longest occupation survey column.Among them, 10,375 subjects without information on work patterns and 5231 subjects without periodontal records, were excluded.Therefore, data from 32,336 (44.08%) participants were used in the final statistical analysis.Among the total survey participants, the group with periodontal disease (Community periodontal index (CPI) ≥ 3) accounted for 41.72%, and the group without periodontal disease (CPI < 3) accounted for 58.28% of the total participants.This study was approved by the institutional review board (IRB) of the Korea University Anam Hospital.(IRB No. 2021AN0047; Seoul, Korea).

Defining sociodemographic, lifestyle variables
Data on sex, age, and the number of missing teeth were recorded.The income level of the respondents was categorized by separating them into quartiles based on the average monthly income of their households.The educational level of the respondents was defined as the highest level of education they had completed.The participants were divided into two groups (smokers and non-smokers) based on their status of smoking at the time of the survey.A professional health researcher completed the questionnaires.Drinking status was classified as non-drinkers, light-to-moderate drinkers (1-30 g/day), and heavy drinkers (> 30 g/day) 16 .Information on sleep duration was collected through self-reported interviews and durations were categorized into three ranges: ≤ 5, 6-8, and ≥ 9 h/day.

Defining metabolic health status
Hypertension (HTN) was defined as blood pressure (BP) ≥ 140/90 mmHg or medication of anti-hypertensive drug at the time of the survey.Prehypertension was defined as BP of 130-139/80-89 mmHg.Fasting blood glucose level of 126 mg/dL or higher was defined as impaired fasting glucose, and diabetes mellitus was defined as impaired fasting glucose and current use of antidiabetic medications.Presence of metabolic syndrome was determined if the participant has three or more of the following criteria fulfilled: (1) waist circumference ≥ 90 cm in males and ≥ 80 cm in females; (2) fasting triglycerides ≥ 150 mg/dl or use of lipid-lowering medication; (3) high-density lipoprotein cholesterol < 40 mg/dl in males and < 50 mg/dl in females or use of medication; (4) BP ≥ 130/85 mmHg or use of antihypertensive medication; and (5) fasting blood glucose ≥ 100 mg/dl or current use of anti-diabetic medication.

Occupational classification, work pattern, and periodontal disease evaluation
The survey on the longest occupation was performed by asking the following question: "What was the occupation you had for the longest duration in your lifetime?"Participants answered the questionnaire based on the nine major classification codes according to the Korean Standard Classification of Occupations and the occupations were mentioned as follows: 1. Managers 2. Professionals and associate professionals 3. Clerks 4. Service workers 5. Shop and market sales workers 6. Skilled agricultural and fishery workers 7. Craft and related trades workers 8. Plant and machine operators and assemblers 9. Elementary occupations Managers, professionals, associate professionals, and clerks, who accounted for 62.99% of the total participants, were re-categorized as white-collar workers.The rest, including service workers, shop and market sales workers, skilled agricultural and fishery workers, craft and related trade workers, plant and machine operators and assemblers, and elementary occupations, were categorized as blue-collar workers.
Daytime work was defined as regular work between 6:00 and 18:00 on weekdays.Shift work included various work schedules, apart from regular daytime work and included evening work, night work, day/night shifts, 24-h shift work, split work, and irregular shift work.Respondents provided information on working hours and shift work based on the occupation they were engaged for the longest period in the lifetime.A total of 14,577 people (45.08%) were employed in daytime work and 17,759 (54.92%) in shift work.
Periodontitis was assessed using the CPI 17 .Periodontal probing depths (PPDs) were measured using CPI probe with a force of 20 g in 10 teeth (tooth numbers 11, 16, 17, 26, 27, 31, 36, 37, 46, and 47).CPI scores were determined based on following criteria: 0, healthy teeth; 1, gingival bleeding after probing; 2, calculus; 3, PPD of 4-5.5 mm; and 4, PPD ≥ 6 mm.Participants who had CPI ≥ 3 in their worst quadrant were considered to have periodontitis.Four public health dentists participated in the oral examinations, and the inter-examiner and inter-examiner reliabilities were higher than the k-coefficient of 0.85.

Statistical analysis
Statistical analysis was performed using the Statistical Analysis System version 9.4.(SAS Institute Inc., Cary, NC, USA).According to the periodontal status of the participants, baseline characteristics were calculated using independent t-test and chi-square test.Data were presented as mean ± standard error and frequency (percentage) for continuous and categorical variables, respectively.Complete case analysis with covariate adjustment was used to handle missing data (Table S3).Statistical significance was set at α = 0.05.

Univariable and multivariable logistic regression
Using univariable logistic regression model, unadjusted crude odd ratios (OR) were calculated for the variables that shows significant differences between CPI < 3 and CPI ≥ 3 groups.Codes were assigned to each group as 0 for CPI < 3, and 1 for CPI ≥ 3. Multivariable logistic regression analysis was performed using the backward elimination method."Change-in-estimate" strategy was applied to identify putative confounders in the model.Variables that show significant increase of the ORs in the univariable model were considered as potential confounders (Table S4).Variables were removed from the model in order of level of significance (= P-value).Variable with the largest P-value was removed in consecutive order, and variables with the significance level > 0.25 were removed from the final model.Interaction effect refers to the role of a variable in an estimated model, and its effect on the dependent variable.When a variable has an interaction effect with some third variable, effects on the dependent variable differs depending on the level of the third variable.In this study, the CONTRAST statement was used to analyze the interaction effects between work patterns and occupation types.Using this interaction term, multiplicative effect of the two variables can be analyzed in multivariable logistic regression model.

Baseline characteristics
Baseline characteristics of the study participants are presented in Table 1 and S1.The mean age of the participants in the periodontitis group was 57.7 ± 13.26 years and the non-periodontitis group was 41.1 ± 13.42 years (P < 0.05).The participants in the periodontitis group had more missing teeth than those in the non-periodontitis group, with an average of 7.9 ± 8.66 versus 1.1 ± 1.8, respectively (P < 0.05).Men (53.87%) were the more affected by periodontitis compared to female (P < 0.05).Variable including BMI, HbA1c, total cholesterol, WBC counts showed significant increases in periodontitis group (P < 0.05).Education, income, smoking, and drinking were also the variables showed significant differences (P < 0.05).Participants with HTN and diabetes occupied in higher percentage within periodontitis group (P < 0.05).In periodontitis group, blue-collar workers accounted for 77.57% and white-collar workers for 22.43% showing significant difference compared to the non-periodontitis group (P < 0.05).Work pattern (shift work/daytime work) also showed significant difference between two groups (P < 0.05).

Univariable logistic regression model
In univariable logistic regression analysis, ORs were calculated to identify potential risk factors for periodontitis.
Variables including age, number or missing teeth, BMI, HbA1c, total cholesterol, WBC count showed positive associations with periodontitis (P < 0.05,

Multivariable logistic regression model
In multivariable logistic regression model, variables including age, BMI, WBC count, gender, education, income, smoking, drinking, and diabetes maintained their significance.For the terms work pattern and occupation, interaction effects were calculated using the CONTRAST statement.When comparison is made between unadjusted ORs (Table 2) and interactions considered adjusted ORs (

Discussion
This study showed that effect of shift work on periodontal status differ according to the occupational types.White-collar workers are more likely to be affected by shift work compared to blue-collar workers in terms of prevalence of periodontitis (OR = 1.381 vs. 1.198,Table 3).This is the result drawn following adjustment for multiple potential confounding factors of periodontal disease including age, gender, BMI, WBC count, education and income level, smoking, drinking, and diabetes 18 .This result is somewhat contrary to general understanding regarding health conditions of blue-and whitecollar workers.According to the previous report, white-collar workers have lower risk for common chronic diseases and lower mortality rate for cardiovascular disease compared to blue-collar workers 19 .Also, in another publication where various risk indicators for chronic disease such as amount of exercise, physical work situation, smoking, diet, cardiorespiratory fitness, BMI, and blood pressure had been considered, blue-collar workers showed to have significantly higher clustering of those risk indicators (OR = 1.80 [1.71-1.90])compared to whitecollar workers 20 .Periodontitis is one of the non-communicable chronic diseases (NCDs) and proved to have close relationship with other NCDs through its contribution to low-grade systemic inflammation 21 .This explains the result of our univariable model revealing increased OR for periodontitis in blue-collar group (OR = 3.123).
The interesting part was to find interaction effect between occupational type and work pattern.Adverse effect of shift work on the periodontal status was greater in white-collar group when comparing to that in blue-collar group (Tables 2 and 3).Crude ORs for blue-collar and shift work group are 3.123 and 1.269, respectively.These numbers change after the interaction term is considered in the model.OR for blue-collar decreases from 3.123 to 1.151 when shift work is engaged, whereas OR for shift work increases in white-collar group from 1.269 to 1.381.
Shift work refers to work schedules apart from regular daytime period and are increasing in numbers as the modern society transforms continuously in accordance with the present needs.Especially, COVID-19 pandemic encouraged the emergence of various telecommuting jobs and invigoration of 24 h delivery industry.Shift work is found to be detrimental to overall health because it inevitably changes one's wake/sleep pattern causing deterioration in sleep quality and disruption of the circadian rhythm 2,6,22 .
Alterations in sleep pattern in a manner which does not correspond to environmental day/night cycle, brings about disruption in one's circadian rhythm.Every living organism has endogenous clock in biological systems such as endocrine, immune, and cardiovascular systems as well as renal and cerebral activities 23 .This clock is restrained by the environment cues like light, feeding, and body temperature.When misalignment is occurred between external and internal circadian clock due to atypical sleep pattern, various physiological activities governed by circadian rhythm cannot function properly.In periodontal aspect, gingival fibroblast, which in charge of first barrier defense at the bacterial front, is found to be regulated by the clock gene CLOCK/BMAL1 24   www.nature.com/scientificreports/White-collar jobs include managers, professionals, associate professionals, and clerks.These workers tend to spend most of their working hours in front of a computer screen, overly exposed to blue light.Since blue-light itself creates a significant disturbance in the circadian rhythm [26][27][28] , combination of shift work and blue-light can be even more harmful.One of the white-collar jobs well known for shift work is the hospital nurses.Their work is strictly engaged to the shift schedules and weakened immunity and poor physical conditions along with such working condition had been reported 29 .However, the exact mechanism of why white-collar workers are more vulnerable to shift work is still ambiguous and a matter for further research.
Nevertheless, the strength of our result is that this is the first study to consider interaction effect between occupational type and shift working pattern.Given the close relationship between periodontal disease and systemic well-being, our result may offer a new perspective to future research regarding shift work and other chronic diseases.
The limitations of this study include its cross-sectional nature, possible underestimation of participants' periodontal status due to the CPI system, and use of self-recorded questionnaires.In addition, several significant data are missing due to the nature of the national surveillance data.Factors like sleep quality, exact duration of the occupational engagement, and oral hygiene status may strengthen the weight of the result.Therefore, further longitudinal study with more detailed data is required in order to confirm the correlation between periodontal disease and the effect of occupational shift work.Also in the future research, categorization of the occupations could be in a different manner, such as white-, blue-, and pink-collar (service and sales workers), for more concrete result.Within the limitations of this study, the effect of shift work seems particularly noticeable in white-collar workers compared to blue-collar workers.The result of this study suggests that 24/7 lifestyle of the modern society poses health risks to the relevant people and the potential harm can be greater to white-collar workers.To determine the range of influence in detail, further investigations with more sophisticated data collection are necessary.
In conclusion, adverse effect of shift work on periodontal disease is greater in white-collar group compared to blue-collar workers.

Table 3
), it is noticeable that following adjustment, OR of shift work for periodontitis decreases in blue-collar group (from 1.269 to1.198 [1.119-1.283]),whereas it increases in white collar (from 1.269 to 1.381[1.253-1.523]).This implies that white-collar workers are affected by shift work to a greater extent compared to blue-collar workers in terms of risk for periodontal disease.Sleep duration was no longer a significant variable in our final model.

Table 1 .
Baseline characteristics of this study according to the presence of periodontitis (N = 32,336).SD, Standard deviation; CPI, community periodontal index.

Table 2 .
Univariable logistic regression analysis producing odds ratio of risk factors for periodontitis.CI, Confidence interval; OR, odds ratio; REF, reference.

Table 3 .
Multivariable logistic regression analysis producing odds ratio of risk factors for periodontitis.CI, Confidence interval; OR, odds ratio; REF, reference.